Investigating how hunger shapes olfactory decision-making in insects

Many insect pests that destroy crops or transmit diseases to millions of people each year rely on their sense of smell to navigate toward their plant or human hosts. As they navigate, crawling insects assess their local odor environment by sweeping their heads before deciding to steer to the left or right. These navigational decisions are influenced by the insect’s hunger state.

This project aims to study how an insect’s hunger state affects its smell neurons, influencing navigational decisions. It takes advantage of the fruit-fly larva as a model system, which allows detailed analyses of smell neurons and their functions. Researchers will use lab-based behavior experiments and advanced molecular and imaging techniques to gather and analyze data.

Expected outcomes of this project include: 1) Enhanced understanding of how hunger affects smell neurons and shapes navigational decisions. 2) Development of an investigative framework to study how multiple satiety hormones, such as insulin and leptin, work together to convey hunger information to smell neurons and influence navigational decisions. 3) Increased understanding of insect navigation strategies, potentially leading to intelligent solutions to combat insect vectors of disease. Additionally, this research will include educational outreach, such as summer workshops for K-12 students from rural counties in Northern Nevada.

These activities are designed to raise awareness of the importance of insects to society and demonstrate how basic science research using insect models can have far-reaching implications for human health. The outreach efforts aim to inspire K-12 students to consider STEM-related careers.

To navigate natural odor environments containing the smells of food and predators, an insect must make navigational decisions balancing the possibilities of reward and danger. Such adaptive decisions are further modulated by the insect’s satiety state. However, the mechanisms modulating the insect’s navigational decision-making remain poorly understood.

Before deciding to navigate to the left or right, a Drosophila larva assesses its odor environment by sweeping its head. Head sweeps, a behavior critical to the larva’s olfactory decision-making, depend on the activity of a pair of inhibitory local neurons in the larval antennal lobe known as Keystone-LN. Keystone-LN-induced head-sweep behavior is affected by the larva’s satiety state; mediated in part via insulin signaling.

This project builds upon these findings: The main objective is to ask how insulin mediates the satiety-dependent changes in Keystone-LN-induced head-sweep behavior in the Drosophila larva. Using state-of-the-art behavior, imaging, and molecular approaches, researchers will test a hypothesis that insulin mediates satiety-dependent changes in larval head-sweep behavior by influencing Keystone-LN’s input and output properties.

First, the investigators will test insulin’s ability to affect Keystone-LN’s input property (odor-evoked response). Next, they will test how and to what extent insulin affects Keystone-LN’s output property, the release of the neurotransmitter GABA. Finally, the downstream components of insulin signaling in Keystone-LN will be identified.

The results will advance our understanding of how adaptability to an internal state is enforced in an inhibitory neuron to shape an insect’s navigational decisions. Understanding these adaptive mechanisms is critical for decoding how neural circuits support animal cognition and behavior.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.